[
International Worm Meeting,
2019]
Do gamete-inherited chromatin states influence gene expression in offspring? This is a burning question in the field and one that remains elusive, in part because it is difficult to determine cause versus consequence when comparing chromatin states with transcriptional status. To test for a cause-effect relationship between inherited chromatin states and offspring transcription we 1) compared genetically identical individuals for different transcriptional outcomes as a result of inheriting different chromatin states, 2) assessed whether transcriptional changes occurred in cis, thus eliminating alternative epigenetic carriers that function in trans (e.g. cytoplasmic ncRNAs), and 3) used the model system C. elegans, which lacks canonical DNA methylation, thus eliminating the alternative epigenetic carrier that also functions in cis. Specifically, we compared transcription in the germline from sperm-inherited and oocyte-inherited alleles in genetically identical worms that inherited the sperm genome with or without the repressive histone modification H3K27me3. Our studies reveal that in C. elegans, sperm-inherited chromatin states directly influence transcription during germline development and protect germ cell identity. Inheritance of a sperm genome without H3K27me3 results in derepression in the germline of many somatic genes, especially neuronal genes, predominantly from sperm-inherited alleles. In a sensitized genetic background, this results in loss of germline-specific markers and reprogramming toward a neuronal fate, as evidenced by expression of neuronal markers and extension of axo-dendritic structures. We found that this reprogramming is progressive and only occurs later in development, indicating that sperm-inherited H3K27me3 serves to protect germ cell identity rather than establish it. Altogether, our findings point to a model in which gamete-inherited patterns of H3K27me3 act as a barrier to inappropriate transcription; in germ cells, this barrier function suppresses transcription of factors that could drive germ cells toward alternative cell identities. These findings demonstrate that histone modifications are one mechanism through which epigenetic information can be passed from father to shape gene expression, development, and fertility in offspring.